Changes in the Milk Metabolome of the Giant Panda (Ailuropoda melanoleuca) with Time after Birth--Three Phases in Early Lactation and Progressive Individual Differences.

Tong Zhang,Liang Zhang,David G Watson,Malcolm W Kennedy,Hairui Wang,Rong Hou,Rong Zhang,I Kati Loeffler,Zhihe Zhang,Daniel Monleon

doi:10.1371/journal.pone.0143417

Abstract

Ursids (bears) in general, and giant pandas in particular, are highly altricial at birth. The components of bear milks and their changes with time may be uniquely adapted to nourish relatively immature neonates, protect them from pathogens, and support the maturation of neonatal digestive physiology. Serial milk samples collected from three giant pandas in early lactation were subjected to untargeted metabolite profiling and multivariate analysis. Changes in milk metabolites with time after birth were analysed by Principal Component Analysis, Hierarchical Cluster Analysis and further supported by Orthogonal Partial Least Square-Discriminant Analysis, revealing three phases of milk maturation: days 1–6 (Phase 1), days 7–20 (Phase 2), and beyond day 20 (Phase 3). While the compositions of Phase 1 milks were essentially indistinguishable among individuals, divergences emerged during the second week of lactation. OPLS regression analysis positioned against the growth rate of one cub tentatively inferred a correlation with changes in the abundance of a trisaccharide, isoglobotriose, previously observed to be a major oligosaccharide in ursid milks. Three artificial milk formulae used to feed giant panda cubs were also analysed, and were found to differ markedly in component content from natural panda milk. These findings have implications for the dependence of the ontogeny of all species of bears, and potentially other members of the Carnivora and beyond, on the complexity and sequential changes in maternal provision of micrometabolites in the immediate period after birth.

Highlights

The chemical complexity of milk required to support neonatal mammalian development is only partially understood
2821 and 1945 liquid chromatography-high resolution mass spectrometry (LC-HRMS) features (pairs of mass to charge ratio (m/z) and retention time) were generated in electrospray ionisation negative and positive mode, respectively, and 368 features were detected in both modes
2199 compounds were characterised on the basis of accurate mass in our in-house database; 93 of these were further identified by matching their retention times with authentic standards (Table C in S1 File)

Summary

Introduction

The chemical complexity of milk required to support neonatal mammalian development is only partially understood. The composition of milks must meet the needs of nursing young at changing developmental stages. The ontogeny of ursid milk is interesting because of the highly altricial nature of bear cubs and the long period of maternal dependence in ursidae. Giant panda cubs in particular are the most altricial of any non-marsupial mammal [4]. While marsupials produce the developmentally most immature neonates of all mammals, Ursidae follow close behind despite a eutherian physiology, taxonomic classification among Carnivora and small litter sizes. Lactation transfers energy in the form of fats to the neonate, which is metabolically much less costly to the mother than the transplacental transfer of glucose to support the foetus [5,6,7]

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